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Published in: Journal of Translational Medicine 1/2017

Open Access 01-12-2017 | Research

Distinct expression profile of HCMV encoded miRNAs in plasma from oral lichen planus patients

Authors: Meng Ding, Xiang Wang, Cheng Wang, Xiaoshuang Liu, Ke Zen, Wenmei Wang, Chen-Yu Zhang, Chunni Zhang

Published in: Journal of Translational Medicine | Issue 1/2017

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Abstract

Background

Oral lichen planus (OLP) is a T cell-mediated autoimmune disease. The aetiology and molecular mechanisms of OLP remain unclear. Human cytomegalovirus (HCMV) infection is a causal factor in the development of various diseases, but the clinical relevance of HCMV in OLP has not been thoroughly investigated.

Methods

In the present study, we firstly examined twenty-three HCMV-encoded microRNA (miRNA) expression profiles in plasma from training set that including 21 OLP patients and 18 healthy controls using RT-qPCR technology. Dysregulated miRNAs were subsequently confirmed in another larger cohort refereed as validation set consisting of 40 OLP patients and 33 healthy controls. HCMV DNA in peripheral blood leukocytes (PBLs) was also measured in an additional cohort of 13 OLP patients and 12 control subjects. Furthermore, bioinformatics analyses, luciferase reporter assay and western blotting were also performed to predict and verify the direct potential targets of HCMV-encoded miRNAs.

Results

The RT-qPCR results showed that the plasma levels of five HCMV-encoded miRNAs including hcmv-miR-UL112-3p, hcmv-miR-UL22a-5p, hcmv-miR-UL148d, hcmv-miR-UL36-5p and hcmv-miR-UL59 were significantly increased in OLP patients in both training and validation sets. HCMV DNA in PBLs was also significantly higher in OLP patients than in control subjects. Additionally, by using a combination of luciferase reporter assay and western blotting, we demonstrated that cytomegalovirus UL16-binding protein 1, a molecule that mediates the killing of virus-infected cells by natural killer cells, is a direct target of hcmv-miR-UL59.

Conclusions

Our results demonstrate a distinct expression pattern of HCMV-encoded miRNAs in OLP patients, which may provide insight into the relationship between HCMV infection and OLP, and warrants additional study in the diagnosis and aetiology of OLP.
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Literature
1.
go back to reference Arao TC, Guimaraes AL, de Paula AM, Gomes CC, Gomez RS. Increased miRNA-146a and miRNA-155 expressions in oral lichen planus. Arch Dermatol Res. 2012;304:371–5.CrossRefPubMed Arao TC, Guimaraes AL, de Paula AM, Gomes CC, Gomez RS. Increased miRNA-146a and miRNA-155 expressions in oral lichen planus. Arch Dermatol Res. 2012;304:371–5.CrossRefPubMed
2.
go back to reference Danielsson K, Ebrahimi M, Wahlin YB, Nylander K, Boldrup L. Increased levels of COX-2 in oral lichen planus supports an autoimmune cause of the disease. J Eur Acad Dermatol Venereol. 2012;26:1415–9.CrossRefPubMed Danielsson K, Ebrahimi M, Wahlin YB, Nylander K, Boldrup L. Increased levels of COX-2 in oral lichen planus supports an autoimmune cause of the disease. J Eur Acad Dermatol Venereol. 2012;26:1415–9.CrossRefPubMed
3.
go back to reference Lodi G, Scully C, Carrozzo M, Griffiths M, Sugerman PB, Thongprasom K. Current controversies in oral lichen planus: report of an international consensus meeting. Part 2. Clinical management and malignant transformation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2005;100:164–78.CrossRefPubMed Lodi G, Scully C, Carrozzo M, Griffiths M, Sugerman PB, Thongprasom K. Current controversies in oral lichen planus: report of an international consensus meeting. Part 2. Clinical management and malignant transformation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2005;100:164–78.CrossRefPubMed
4.
go back to reference Hu JY, Zhang J, Cui JL, Liang XY, Lu R, Du GF, Xu XY, Zhou G. Increasing CCL5/CCR5 on CD4+ T cells in peripheral blood of oral lichen planus. Cytokine. 2013;62:141–5.CrossRefPubMed Hu JY, Zhang J, Cui JL, Liang XY, Lu R, Du GF, Xu XY, Zhou G. Increasing CCL5/CCR5 on CD4+ T cells in peripheral blood of oral lichen planus. Cytokine. 2013;62:141–5.CrossRefPubMed
5.
go back to reference Liu GX, Sun JT, Yang MX, Qi XM, Shao QQ, Xie Q, Qu X, Wei FC, Sun SZ. OPN promotes survival of activated T cells by up-regulating CD44 in patients with oral lichen planus. Clin Immunol. 2011;138:291–8.CrossRefPubMed Liu GX, Sun JT, Yang MX, Qi XM, Shao QQ, Xie Q, Qu X, Wei FC, Sun SZ. OPN promotes survival of activated T cells by up-regulating CD44 in patients with oral lichen planus. Clin Immunol. 2011;138:291–8.CrossRefPubMed
6.
7.
go back to reference Huang CT, Oyang YJ, Huang HC, Juan HF. MicroRNA-mediated networks underlie immune response regulation in papillary thyroid carcinoma. Sci Rep. 2014;4:6495.CrossRefPubMedPubMedCentral Huang CT, Oyang YJ, Huang HC, Juan HF. MicroRNA-mediated networks underlie immune response regulation in papillary thyroid carcinoma. Sci Rep. 2014;4:6495.CrossRefPubMedPubMedCentral
8.
go back to reference Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435:834–8.CrossRefPubMed Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435:834–8.CrossRefPubMed
9.
10.
go back to reference Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008;18:997–1006.CrossRefPubMed Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008;18:997–1006.CrossRefPubMed
11.
go back to reference Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O’Briant KC, Allen A, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105:10513–8.CrossRefPubMedPubMedCentral Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O’Briant KC, Allen A, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105:10513–8.CrossRefPubMedPubMedCentral
12.
go back to reference Soderberg-Naucler C, Nelson JY. Human cytomegalovirus latency and reactivation—a delicate balance between the virus and its host’s immune system. Intervirology. 1999;42:314–21.CrossRefPubMed Soderberg-Naucler C, Nelson JY. Human cytomegalovirus latency and reactivation—a delicate balance between the virus and its host’s immune system. Intervirology. 1999;42:314–21.CrossRefPubMed
13.
go back to reference Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, Tuschl T. Identification of virus-encoded microRNAs. Science. 2004;304:734–6.CrossRefPubMed Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, Tuschl T. Identification of virus-encoded microRNAs. Science. 2004;304:734–6.CrossRefPubMed
14.
go back to reference Baryawno N, Rahbar A, Wolmer-Solberg N, Taher C, Odeberg J, Darabi A, Khan Z, Sveinbjornsson B, FuskevAg OM, Segerstrom L, et al. Detection of human cytomegalovirus in medulloblastomas reveals a potential therapeutic target. J Clin Invest. 2011;121:4043–55.CrossRefPubMedPubMedCentral Baryawno N, Rahbar A, Wolmer-Solberg N, Taher C, Odeberg J, Darabi A, Khan Z, Sveinbjornsson B, FuskevAg OM, Segerstrom L, et al. Detection of human cytomegalovirus in medulloblastomas reveals a potential therapeutic target. J Clin Invest. 2011;121:4043–55.CrossRefPubMedPubMedCentral
15.
go back to reference Fielding CA, Aicheler R, Stanton RJ, Wang EC, Han S, Seirafian S, Davies J, McSharry BP, Weekes MP, Antrobus PR, et al. Two novel human cytomegalovirus NK cell evasion functions target MICA for lysosomal degradation. PLoS Pathog. 2014;10:e1004058.CrossRefPubMedPubMedCentral Fielding CA, Aicheler R, Stanton RJ, Wang EC, Han S, Seirafian S, Davies J, McSharry BP, Weekes MP, Antrobus PR, et al. Two novel human cytomegalovirus NK cell evasion functions target MICA for lysosomal degradation. PLoS Pathog. 2014;10:e1004058.CrossRefPubMedPubMedCentral
16.
go back to reference Pavelin J, Reynolds N, Chiweshe S, Wu G, Tiribassi R, Grey F. Systematic microRNA analysis identifies ATP6V0C as an essential host factor for human cytomegalovirus replication. PLoS Pathog. 2013;9:e1003820.CrossRefPubMedPubMedCentral Pavelin J, Reynolds N, Chiweshe S, Wu G, Tiribassi R, Grey F. Systematic microRNA analysis identifies ATP6V0C as an essential host factor for human cytomegalovirus replication. PLoS Pathog. 2013;9:e1003820.CrossRefPubMedPubMedCentral
17.
go back to reference Grey F, Tirabassi R, Meyers H, Wu G, McWeeney S, Hook L, Nelson JA. A viral microRNA down-regulates multiple cell cycle genes through mRNA 5′UTRs. PLoS Pathog. 2010;6:e1000967.CrossRefPubMedPubMedCentral Grey F, Tirabassi R, Meyers H, Wu G, McWeeney S, Hook L, Nelson JA. A viral microRNA down-regulates multiple cell cycle genes through mRNA 5′UTRs. PLoS Pathog. 2010;6:e1000967.CrossRefPubMedPubMedCentral
18.
go back to reference Li S, Zhu J, Zhang W, Chen Y, Zhang K, Popescu LM, Ma X, Lau WB, Rong R, Yu X, et al. Signature microRNA expression profile of essential hypertension and its novel link to human cytomegalovirus infection. Circulation. 2011;124:175–84.CrossRefPubMed Li S, Zhu J, Zhang W, Chen Y, Zhang K, Popescu LM, Ma X, Lau WB, Rong R, Yu X, et al. Signature microRNA expression profile of essential hypertension and its novel link to human cytomegalovirus infection. Circulation. 2011;124:175–84.CrossRefPubMed
19.
go back to reference Mohammad AA, Rahbar A, Lui WO, Davoudi B, Catrina A, Stragliotto G, Mellbin L, Hamsten A, Ryden L, Yaiw KC, Soderberg-Naucler C. Detection of circulating hcmv-miR-UL112-3p in patients with glioblastoma, rheumatoid arthritis, diabetes mellitus and healthy controls. PLoS ONE. 2014;9:e113740.CrossRefPubMedPubMedCentral Mohammad AA, Rahbar A, Lui WO, Davoudi B, Catrina A, Stragliotto G, Mellbin L, Hamsten A, Ryden L, Yaiw KC, Soderberg-Naucler C. Detection of circulating hcmv-miR-UL112-3p in patients with glioblastoma, rheumatoid arthritis, diabetes mellitus and healthy controls. PLoS ONE. 2014;9:e113740.CrossRefPubMedPubMedCentral
20.
go back to reference Kim S, Lee S, Shin J, Kim Y, Evnouchidou I, Kim D, Kim YK, Kim YE, Ahn JH, Riddell SR, et al. Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1. Nat Immunol. 2011;12:984–91.CrossRefPubMedPubMedCentral Kim S, Lee S, Shin J, Kim Y, Evnouchidou I, Kim D, Kim YK, Kim YE, Ahn JH, Riddell SR, et al. Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1. Nat Immunol. 2011;12:984–91.CrossRefPubMedPubMedCentral
21.
go back to reference Pan Y, Wang N, Zhou Z, Liang H, Pan C, Zhu D, Liu F, Zhang CY, Zhang Y, Zen K. Circulating human cytomegalovirus-encoded HCMV-miR-US4-1 as an indicator for predicting the efficacy of IFNalpha treatment in chronic hepatitis B patients. Sci Rep. 2016;6:23007.CrossRefPubMedPubMedCentral Pan Y, Wang N, Zhou Z, Liang H, Pan C, Zhu D, Liu F, Zhang CY, Zhang Y, Zen K. Circulating human cytomegalovirus-encoded HCMV-miR-US4-1 as an indicator for predicting the efficacy of IFNalpha treatment in chronic hepatitis B patients. Sci Rep. 2016;6:23007.CrossRefPubMedPubMedCentral
22.
go back to reference Ghodratnama F, Wray D, Bagg J. Detection of serum antibodies against cytomegalovirus, varicella zoster virus and human herpesvirus 6 in patients with recurrent aphthous stomatitis. J Oral Pathol Med. 1999;28:12–5.CrossRefPubMed Ghodratnama F, Wray D, Bagg J. Detection of serum antibodies against cytomegalovirus, varicella zoster virus and human herpesvirus 6 in patients with recurrent aphthous stomatitis. J Oral Pathol Med. 1999;28:12–5.CrossRefPubMed
23.
go back to reference Zhang C, Wang C, Chen X, Yang C, Li K, Wang J, Dai J, Hu Z, Zhou X, Chen L, et al. Expression profile of microRNAs in serum: a fingerprint for esophageal squamous cell carcinoma. Clin Chem. 2010;56:1871–9.CrossRefPubMed Zhang C, Wang C, Chen X, Yang C, Li K, Wang J, Dai J, Hu Z, Zhou X, Chen L, et al. Expression profile of microRNAs in serum: a fingerprint for esophageal squamous cell carcinoma. Clin Chem. 2010;56:1871–9.CrossRefPubMed
24.
go back to reference Wang C, Hu J, Lu M, Gu H, Zhou X, Chen X, Zen K, Zhang CY, Zhang T, Ge J, et al. A panel of five serum miRNAs as a potential diagnostic tool for early-stage renal cell carcinoma. Sci Rep. 2015;5:7610.CrossRefPubMedPubMedCentral Wang C, Hu J, Lu M, Gu H, Zhou X, Chen X, Zen K, Zhang CY, Zhang T, Ge J, et al. A panel of five serum miRNAs as a potential diagnostic tool for early-stage renal cell carcinoma. Sci Rep. 2015;5:7610.CrossRefPubMedPubMedCentral
25.
go back to reference Sousa FA, Rosa LE. Oral lichen planus: clinical and histopathological considerations. Braz J Otorhinolaryngol. 2008;74:284–92.CrossRefPubMed Sousa FA, Rosa LE. Oral lichen planus: clinical and histopathological considerations. Braz J Otorhinolaryngol. 2008;74:284–92.CrossRefPubMed
26.
go back to reference Zhang S, Zhou YH, Li L, Hu Y. Monitoring human cytomegalovirus infection with nested PCR: comparison of positive rates in plasma and leukocytes and with quantitative PCR. Virol J. 2010;7:73.CrossRefPubMedPubMedCentral Zhang S, Zhou YH, Li L, Hu Y. Monitoring human cytomegalovirus infection with nested PCR: comparison of positive rates in plasma and leukocytes and with quantitative PCR. Virol J. 2010;7:73.CrossRefPubMedPubMedCentral
27.
go back to reference Pellegrin I, Garrigue I, Ekouevi D, Couzi L, Merville P, Merel P, Chene G, Schrive MH, Trimoulet P, Lafon ME, Fleury H. New molecular assays to predict occurrence of cytomegalovirus disease in renal transplant recipients. J Infect Dis. 2000;182:36–42.CrossRefPubMed Pellegrin I, Garrigue I, Ekouevi D, Couzi L, Merville P, Merel P, Chene G, Schrive MH, Trimoulet P, Lafon ME, Fleury H. New molecular assays to predict occurrence of cytomegalovirus disease in renal transplant recipients. J Infect Dis. 2000;182:36–42.CrossRefPubMed
28.
go back to reference Nachmani D, Lankry D, Wolf DG, Mandelboim O. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat Immunol. 2010;11:806–13.CrossRefPubMed Nachmani D, Lankry D, Wolf DG, Mandelboim O. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat Immunol. 2010;11:806–13.CrossRefPubMed
29.
go back to reference Kim Y, Lee S, Kim S, Kim D, Ahn JH, Ahn K. Human cytomegalovirus clinical strain-specific microRNA miR-UL148D targets the human chemokine RANTES during infection. PLoS Pathog. 2012;8:e1002577.CrossRefPubMedPubMedCentral Kim Y, Lee S, Kim S, Kim D, Ahn JH, Ahn K. Human cytomegalovirus clinical strain-specific microRNA miR-UL148D targets the human chemokine RANTES during infection. PLoS Pathog. 2012;8:e1002577.CrossRefPubMedPubMedCentral
30.
go back to reference Hook LM, Grey F, Grabski R, Tirabassi R, Doyle T, Hancock M, Landais I, Jeng S, McWeeney S, Britt W, Nelson JA. Cytomegalovirus miRNAs target secretory pathway genes to facilitate formation of the virion assembly compartment and reduce cytokine secretion. Cell Host Microbe. 2014;15:363–73.CrossRefPubMedPubMedCentral Hook LM, Grey F, Grabski R, Tirabassi R, Doyle T, Hancock M, Landais I, Jeng S, McWeeney S, Britt W, Nelson JA. Cytomegalovirus miRNAs target secretory pathway genes to facilitate formation of the virion assembly compartment and reduce cytokine secretion. Cell Host Microbe. 2014;15:363–73.CrossRefPubMedPubMedCentral
31.
go back to reference Lisboa LF, Egli A, O’Shea D, Asberg A, Hartmann A, Rollag H, Pang XL, Tyrrell DL, Kumar D, Humar A. Hcmv-miR-UL22A-5p: a biomarker in transplantation with broad impact on host gene expression and potential immunological implications. Am J Transplant. 2015;15:1893–902.CrossRefPubMed Lisboa LF, Egli A, O’Shea D, Asberg A, Hartmann A, Rollag H, Pang XL, Tyrrell DL, Kumar D, Humar A. Hcmv-miR-UL22A-5p: a biomarker in transplantation with broad impact on host gene expression and potential immunological implications. Am J Transplant. 2015;15:1893–902.CrossRefPubMed
32.
go back to reference Kawano Y, Kawada J, Kamiya Y, Suzuki M, Torii Y, Kimura H, Ito Y. Analysis of circulating human and viral microRNAs in patients with congenital cytomegalovirus infection. J Perinatol. 2016;36:1101–5.CrossRefPubMed Kawano Y, Kawada J, Kamiya Y, Suzuki M, Torii Y, Kimura H, Ito Y. Analysis of circulating human and viral microRNAs in patients with congenital cytomegalovirus infection. J Perinatol. 2016;36:1101–5.CrossRefPubMed
33.
go back to reference Lucin P, Mahmutefendic H, Blagojevic Zagorac G, Ilic Tomas M. Cytomegalovirus immune evasion by perturbation of endosomal trafficking. Cell Mol Immunol. 2015;12:154–69.CrossRefPubMed Lucin P, Mahmutefendic H, Blagojevic Zagorac G, Ilic Tomas M. Cytomegalovirus immune evasion by perturbation of endosomal trafficking. Cell Mol Immunol. 2015;12:154–69.CrossRefPubMed
34.
go back to reference Seidel E, Le VT, Bar-On Y, Tsukerman P, Enk J, Yamin R, Stein N, Schmiedel D, Djian EO, Weisblum Y, Tirosh B. Dynamic co-evolution of host and pathogen: HCMV downregulates the prevalent allele MICA *008 to escape elimination by NK cells. Cell Reports. 2015;10:968–82.CrossRef Seidel E, Le VT, Bar-On Y, Tsukerman P, Enk J, Yamin R, Stein N, Schmiedel D, Djian EO, Weisblum Y, Tirosh B. Dynamic co-evolution of host and pathogen: HCMV downregulates the prevalent allele MICA *008 to escape elimination by NK cells. Cell Reports. 2015;10:968–82.CrossRef
35.
go back to reference Eagle RA, Trowsdale J. Promiscuity and the single receptor: NKG2D. Nat Rev Immunol. 2007;7:737–44.CrossRefPubMed Eagle RA, Trowsdale J. Promiscuity and the single receptor: NKG2D. Nat Rev Immunol. 2007;7:737–44.CrossRefPubMed
36.
go back to reference Halenius A, Gerke C, Hengel H. Classical and non-classical MHC I molecule manipulation by human cytomegalovirus: so many targets-but how many arrows in the quiver? Cell Mol Immunol. 2015;12:139–53.CrossRefPubMed Halenius A, Gerke C, Hengel H. Classical and non-classical MHC I molecule manipulation by human cytomegalovirus: so many targets-but how many arrows in the quiver? Cell Mol Immunol. 2015;12:139–53.CrossRefPubMed
37.
go back to reference Dunn C, Chalupny NJ, Sutherland CL, Dosch S, Sivakumar PV, Johnson DC, Cosman D. Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J Exp Med. 2003;197:1427–39.CrossRefPubMedPubMedCentral Dunn C, Chalupny NJ, Sutherland CL, Dosch S, Sivakumar PV, Johnson DC, Cosman D. Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J Exp Med. 2003;197:1427–39.CrossRefPubMedPubMedCentral
38.
go back to reference Cosman D, Mullberg J, Sutherland CL, Chin W, Armitage R, Fanslow W, Kubin M, Chalupny NJ. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity. 2001;14:123–33.CrossRefPubMed Cosman D, Mullberg J, Sutherland CL, Chin W, Armitage R, Fanslow W, Kubin M, Chalupny NJ. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity. 2001;14:123–33.CrossRefPubMed
39.
go back to reference Gallo A, Tandon M, Alevizos I, Illei GG. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS ONE. 2012;7:e30679.CrossRefPubMedPubMedCentral Gallo A, Tandon M, Alevizos I, Illei GG. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS ONE. 2012;7:e30679.CrossRefPubMedPubMedCentral
40.
go back to reference Xu D, Tahara H. The role of exosomes and microRNAs in senescence and aging. Adv Drug Deliv Rev. 2013;65:368–75.CrossRefPubMed Xu D, Tahara H. The role of exosomes and microRNAs in senescence and aging. Adv Drug Deliv Rev. 2013;65:368–75.CrossRefPubMed
41.
go back to reference Li L, Zhu D, Huang L, Zhang J, Bian Z, Chen X, Liu Y, Zhang CY, Zen K. Argonaute 2 complexes selectively protect the circulating microRNAs in cell-secreted microvesicles. PLoS ONE. 2012;7:e46957.CrossRefPubMedPubMedCentral Li L, Zhu D, Huang L, Zhang J, Bian Z, Chen X, Liu Y, Zhang CY, Zen K. Argonaute 2 complexes selectively protect the circulating microRNAs in cell-secreted microvesicles. PLoS ONE. 2012;7:e46957.CrossRefPubMedPubMedCentral
44.
go back to reference Miyamoto M, Fujita T, Kimura Y, Maruyama M, Harada H, Sudo Y, Miyata T, Taniguchi T. Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-beta gene regulatory elements. Cell. 1988;54:903–13.CrossRefPubMed Miyamoto M, Fujita T, Kimura Y, Maruyama M, Harada H, Sudo Y, Miyata T, Taniguchi T. Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-beta gene regulatory elements. Cell. 1988;54:903–13.CrossRefPubMed
45.
go back to reference Wang YP, Qi Y, Huang YJ, Qi ML, Ma YP, He R, Ji YH, Sun ZR, Ruan Q. Identification of immediate early gene X-1 as a cellular target gene of hcmv-mir-UL148D. Int J Mol Med. 2013;31:959–66.PubMed Wang YP, Qi Y, Huang YJ, Qi ML, Ma YP, He R, Ji YH, Sun ZR, Ruan Q. Identification of immediate early gene X-1 as a cellular target gene of hcmv-mir-UL148D. Int J Mol Med. 2013;31:959–66.PubMed
Metadata
Title
Distinct expression profile of HCMV encoded miRNAs in plasma from oral lichen planus patients
Authors
Meng Ding
Xiang Wang
Cheng Wang
Xiaoshuang Liu
Ke Zen
Wenmei Wang
Chen-Yu Zhang
Chunni Zhang
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2017
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-017-1222-8

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